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Population genetics reveals divergent lineages and ongoing hybridization in a declining migratory fish species complex

Abstract

Deciphering the effects of historical and recent demographic processes responsible for the spatial patterns of genetic diversity and structure is a key objective in evolutionary and conservation biology. Using population genetic analyses, we investigated the demographic history, the contemporary genetic diversity and structure, and the occurrence of hybridization and introgression of two species of anadromous fish with contrasting life history strategies and which have undergone recent demographic declines, the allis shad (Alosa alosa) and the twaite shad (Alosa fallax). We genotyped 706 individuals from 20 rivers and 5 sites at sea in Southern Europe at thirteen microsatellite markers. Genetic structure between populations was lower for the nearly semelparous species A. alosa, which disperses greater distances compared to the iteroparous species, A. fallax. Individuals caught at sea were assigned at the river level for A. fallax and at the region level for A. alosa. Using an approximate Bayesian computation framework, we inferred that the most likely long term historical divergence scenario between both species and lineages involved historical separation followed by secondary contact accompanied by strong population size decline. Accordingly, we found evidence for contemporary hybridization and bidirectional introgression due to gene flow between both species and lineages. Moreover, our results support the existence of at least one distinct species in the Mediterrannean sea: A. agone in Golfe du Lion area, and another divergent lineage in Corsica. Overall, our results shed light on the interplay between historical and recent demographic processes and life history strategies in shaping population genetic diversity and structure of closely related species. The recent demographic decline of these species’ populations and their hybridization should be carefully considered while implementing conservation programs.

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Fig. 1: Map showing the location of sampling sites across France, United-Kingdom and Spain.
Fig. 2: Contrasted population genetic structure in the highly dispersive species (A. alosa) compared to the less dispersive species (A. fallax).
Fig. 3: Isolation by distance and phylogenetic clustering.
Fig. 4: Model of divergence and prior and posterior distribution of paramater estimates.

Data availability

Data are deposited on dryad (https://doi.org/10.5061/dryad.rn8pk0pdb) and code for ABC simulations are available on github https://github.com/QuentinRougemont/MicrosatDemogInference.

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Acknowledgements

We thank the many professional fishermen involved in gathering samples. We thank the institutions involved in collecting samples, namely people at INRAE, OFB and FDPPMA 14, 22, 50, and Migado association. We thank A. Xuereb for extensive revision of the manuscript grammar. This study was funded by the European Regional Development Fund (Transnational program Interreg IV. Atlantic Aquatic Resource Conservation Project).

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Conception: QR, GE, SL, JLB; Data Collection: QR, IL, YA, EL, EF, ER, FC, DJN, JLB; Molecular Laboratory: QR, ALB, SL; Data Analysis: QR, CP; Writing first draft: QR with help from SL and DJN; Reviewing: QR with input from all authors.

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Correspondence to Quentin Rougemont.

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Rougemont, Q., Perrier, C., Besnard, AL. et al. Population genetics reveals divergent lineages and ongoing hybridization in a declining migratory fish species complex. Heredity 129, 137–151 (2022). https://doi.org/10.1038/s41437-022-00547-9

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